Growth of northern deciduous trees under increasing atmospheric humidity: possible mechanisms behind the growth retardation

Abstract

Increasing atmospheric humidity—a climate trend predicted for northern Europe—will reduce water flux through vegetation. Diminished transpirational water flux impacts various physiological processes, causing growth decline in deciduous trees. We propose, based on the results obtained from the long-term free air humidity manipulation experiment, concurrent mechanisms to explain the growth deceleration due to increases in relative air humidity. Reduced atmospheric evaporative demand diminishes nutrient uptake and leads to lower leaf nutritional status and to an unbalanced foliar phosphorus/nitrogen ratio (P:N), resulting in a decline in leaf photosynthetic capacity. Elevated relative humidity induces readjustment of foliar metabolism: disturbed N metabolism, accumulation of starch and changes in secondary metabolite contents probably impair both photosynthetic performance and growth. Increased carbohydrate content in the leaves suggests that sink strength of trees is reduced under elevated humidity. As a consequence of the stress, foliar development is hindered, observed at individual leaf or whole-tree foliage levels, lowering production potential of trees proportionally to their foliar area. Larger investments in stem xylem in relation to foliage cause an increase in the ratio of non-photosynthetic to photosynthetic tissues, leading to larger maintenance respiration costs determined by the volume of parenchymatous tissue. An increase in the proportion of living parenchyma cells in relation to dead xylem elements in sapwood additionally enhances respiration costs. Disproportionate changes in hydraulic versus stomatal conductance become a critical factor in the case of weather extremes, which limit canopy conductance and may induce dysfunction of the hydraulic system. Increasing environmental humidity creates favourable conditions for development of pathogens, increasing frequency of fungal damage.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aasamaa K, Kõivik K, Kupper P, Sõber A (2014) Growth environment determines light sensitivity of shoot hydraulic conductance. Ecol Res 29:143–151. doi:10.1007/s11284-013-1104-3

    Article  Google Scholar 

  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67. doi:10.1016/S0065-2504(08)60016-1

    CAS  Google Scholar 

  3. Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372. doi:10.1111/j.1469-8137.2004.01224.x

    Article  Google Scholar 

  4. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684. doi:10.1016/j.foreco.2009.09.001

    Article  Google Scholar 

  5. Bengough AG (2011) Root responses to soil physical limitations. In: Gliński J, Horabik J, Jerzy Lipiec J (eds) Encyclopedia of agrophysics. Springer, Dordrecht, pp 709–712. doi:10.1007/978-90-481-3585-1

  6. Bovard BD, Curtis PS, Vogel CS, Su H-B, Schmid HP (2005) Environmental controls on sap flow in a northern hardwood forest. Tree Physiol 25:31–38. doi:10.1093/treephys/25.1.31

    CAS  Article  Google Scholar 

  7. Bown HE, Watt MS, Clinton PW, Mason EG, Richardson B (2007) Partitioning concurrent influences of nitrogen and phosphorus supply on photosynthetic model parameters of Pinus radiata. Tree Physiol 27:335–344. doi:10.1093/treephys/27.3.335

    CAS  Article  Google Scholar 

  8. Brinson MM, Bradshaw HD, Kane ES (1984) Nutrient assimilative capacity of an alluvial floodplain swamp. J Appl Ecol 21:1041–1157. doi:10.2307/2405066

    Article  Google Scholar 

  9. Bussoti F, Pollastrini M, Holland V, Brüggemann W (2015) Functional traits and adaptive capacity of European forests to climate change. Environ Exp Bot 111:91–113. doi:10.1016/j.envexpbot.2014.11.006

    Article  Google Scholar 

  10. Carey EV, Callaway RM, DeLucia EH (1997) Stem respiration of ponderosa pines grown in contrasting climates: implications for global climate change. Oecologia 111:19–25. doi:10.1007/s004420050203

    Article  Google Scholar 

  11. Cernusak LA, Winter K, Turner BL (2011) Transpiration modulates phosphorus acquisition in tropical tree seedlings. Tree Physiol 31:878–885. doi:10.1093/treephys/tpr077

    Article  Google Scholar 

  12. Ceschia É, Damesin C, Lebaube S, Pontailler J-Y, Dufrêne É (2002) Spatial and seasonal variations in stem respiration of beech trees (Fagus sylvatica). Ann For Sci 59:801–812. doi:10.1051/forest:2002078

    Article  Google Scholar 

  13. Cramer MD, Hawkins H-J, Verboom GA (2009) The importance of nutritional regulation of plant water flux. Oecologia 161:15–24. doi:10.1007/s00442-009-1364-3

    Article  Google Scholar 

  14. DeLucia EH, Drake JE, Thomas RB, Gonzalez-Meler M (2007) Forest carbon use efficiency: Is respiration a constant fraction of gross primary production? Glob Change Biol 13:1157–1167. doi:10.1111/j.1365-2486.2007.01365.x

    Article  Google Scholar 

  15. Desprez-Loustau M-L, Marçais B, Nageleisen L-M, Piou D, Vannini A (2006) Interactive effects of drought and pathogens in forest trees. Ann For Sci 63:597–612. doi:10.1051/forest:2006040

    Article  Google Scholar 

  16. Di Ferdinando M, Brunetti C, Fini A, Tattini M (2012) Flavonoids as antioxidants in plants under abiotic stress. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants. Metabolism, productivity and sustainability. Springer, New York, pp 159-179. doi: 10.1007/978-1-4614-0634-1_9

  17. Dreyer E (1994) Compared sensitivity of seedlings from 3 woody species (Quercus robur L., Quercus rubra L. and Fagus silvatica L.) to water-logging and associated root hypoxia: effects on water relations and photosynthesis. Ann For Sci 51:417–429. doi:10.1051/forest:19940407

    Article  Google Scholar 

  18. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074. doi:10.1126/science.289.5487.2068

    CAS  Article  Google Scholar 

  19. Esteban LG, Martín JA, de Palacios P, Fernández FG (2012) Influence of region of provenance and climate factors on wood anatomical traits of Pinus nigra Arn. subp. salzmannii. Eur J For Res 131:633–645. doi:10.1007/s10342-011-0537-x

    Article  Google Scholar 

  20. Evans RY, Hansen J, Dodge LL (2009) Growth of rose roots and shoots is highly sensitive to anaerobic or hypoxic regions of container substrates. Sci Hortic 119:286–291. doi:10.1016/j.scienta.2008.07.033

    CAS  Article  Google Scholar 

  21. Fonti P, Heller O, Cherubini A, Rigling A, Arend M (2013) Wood anatomical responses of oak saplings to air warming and soil drought. Plant Biol 15(Suppl. 1):210–219. doi:10.1111/j.1438-8677.2012.00599.x

    Article  Google Scholar 

  22. Fritz C, Palacios-Rojas N, Feil R, Stitt M (2006) Regulation of secondary metabolism by the carbon–nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J 46:533–548. doi:10.1111/j.1365-313X.2006.02715.x

    CAS  Article  Google Scholar 

  23. Gartner LG, Baker DC, Spicer R (2000) Distribution and vitality of xylem rays in relation to tree leaf area in Douglas fir. IAWA J 21:389–401. doi:10.1163/22941932-90000255

    Article  Google Scholar 

  24. Gauthier S, Bernier P, Kuuluvainen T, Shvidenko AZ, Schepaschenko DG (2015) Boreal forest health and global change. Science 349:819–822. doi:10.1126/science.aaa9092

    CAS  Article  Google Scholar 

  25. Godbold D, Tullus A, Kupper P, Sõber J, Ostonen I, Godbold JA, Lukac M, Ahmed IU, Smith AR (2014) Elevated atmospheric CO2 and humidity delay leaf fall in Betula pendula, but not in Alnus glutinosa or Populus tremula × tremuloides. Ann For Sci 71:831–842. doi:10.1007/s13595-014-0382-4

    Article  Google Scholar 

  26. Hacke UG, Plavcová L, Almeida-Rodriguez A, King-Jones S, Zhou W, Cooke JEK (2010) Influence of nitrogen fertilization on xylem traits and aquaporin expression in stems of hybrid poplar. Tree Physiol 30:1016–1025. doi:10.1093/treephys/tpq058

    CAS  Article  Google Scholar 

  27. Hansen R, Mander Ü, Soosaar K, Maddison M, Lõhmus K, Kupper P, Kanal A, Sõber J (2013) Greenhouse gas fluxes in an open air humidity manipulation experiment. Landscape Ecol 28:637–649. doi:10.1007/s10980-012-9775-7

    Article  Google Scholar 

  28. Hanso M, Drenkhan R (2010) Two new Ascomycetes on twigs and leaves of Silver birches (Betula pendula) in Estonia. Folia Cryptog Estonica 47:21–26

    Google Scholar 

  29. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162. doi:10.1126/science.1063699

    CAS  Article  Google Scholar 

  30. Herrera A (2013) Responses to flooding of plant water relations and leaf gas exchange in tropical tolerant trees of a black-water wetland. Front Plant Sci 4:106. doi:10.3389/fpls.2013.00106

    CAS  Article  Google Scholar 

  31. Hölscher D, Koch O, Korn S, Leuschner C (2005) Sap flux of five co-occurring tree species in a temperate broad-leaved forest during seasonal soil drought. Trees 19:628–637. doi:10.1007/s00468-005-0426-3

    Article  Google Scholar 

  32. IPCC (2013) Climate change 2013: the physical science basis. Cambridge University Press, Cambridge

    Google Scholar 

  33. Islam MA, Macdonald SE (2009) Current uptake of 15N–labeled ammonium and nitrate in flooded and non-flooded black spruce and tamarack seedlings. Ann For Sci 66:102. doi:10.1051/forest:2008077

    Article  CAS  Google Scholar 

  34. Jacob D, Petersen J, Eggert B, Alias A, Christensen OB, Bouwer LM, Braun A, Colette A, Déqué M, Georgievski G, Georgopolou E, Gobiet A, Menut L, Nikulin G, Haensler A, Hempelmann N, Jones C, Keuler K, Kovats S, Kröner N, Kotlarski S, Kriegsmann A, Martin E, Meijgaard E, Moseley C, Pfeifer S, Preuschmann S, Radermacher C, Radke K, Rechid D, Rounsevell M, Samuelsson P, Somot S, Soussana J-F, Teichmann C, Valentini R, Vautard R, Weber B, Yiou P (2014) EURO-CORDEX: new high-resolution climate change projections for European impact research. Reg Environ Change 14:563–578. doi:10.1007/s10113-013-0499-2

    Article  Google Scholar 

  35. Jarvis P, Linder S (2000) Constraints to growth of boreal forests. Nature 405:904–905. doi:10.1038/35016154

    CAS  Article  Google Scholar 

  36. Jasińska AK, Alber M, Tullus A, Rahi M, Sellin A (2015) Impact of elevated atmospheric humidity on anatomical and hydraulic traits of xylem in hybrid aspen. Funct Plant Biol 42:565–578. doi:10.1071/FP14224

    Article  CAS  Google Scholar 

  37. Jones HG (2010) Can water droplets on leaves cause leaf scorch? New Phytol 185:865–867. doi:10.1111/j.1469-8137.2009.03161.x

    Article  Google Scholar 

  38. Kellomäki S, Wang K-Y (2001) Growth and resource use of birch seedlings under elevated carbon dioxide and temperature. Ann Bot 87:669–682. doi:10.1006/anbo.2001.1393

    Article  CAS  Google Scholar 

  39. Kirakosyan A, Kaufman P, Warber S, Zick S, Aaronson K, Bolling S, Chang SC (2004) Applied environmental stresses to enhance the levels of polyphenolics in leaves of hawthorn plants. Physiol Plant 121:182–186. doi:10.1111/j.1399-3054.2004.00332.x

    CAS  Article  Google Scholar 

  40. Koch GW, Sillett SC, Antoine ME, Williams CB (2015) Growth maximization trumps maintenance of leaf conductance in the tallest angiosperm. Oecologia 177:321–331. doi:10.1007/s00442-014-3181-6

    Article  Google Scholar 

  41. Koricheva J, Larsson S, Haukioja E, Keinänen M (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos 83:212–226. doi:10.2307/3546833

    CAS  Article  Google Scholar 

  42. Kozlowski TT (1982) Water supply and tree growth. Part II Flooding. For Abstr 43:145–161

    Google Scholar 

  43. Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiol Monogr 1:1–29

    Google Scholar 

  44. Kramer PJ, Boyer JS (1995) Water relations of plants and soil. Academic Press, San Diego

    Google Scholar 

  45. Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ 37:2245–2259. doi:10.1111/pce.12310

    CAS  Google Scholar 

  46. Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473. doi:10.1104/pp.108.125989

    CAS  Article  Google Scholar 

  47. Kukk M, Räim O, Tulva I, Sõber J, Lõhmus K, Sõber A (2015) Elevated air humidity modulates bud size and the frequency of bud break in fast-growing deciduous trees: silver birch (Betula pendula Roth.) and hybrid aspen (Populus tremula L. × P. tremuloides Michx.). Trees 29:1381–1393. doi:10.1007/s00468-015-1215-2

    Article  Google Scholar 

  48. Kukumägi M, Ostonen I, Kupper P, Truu M, Tulva I, Varik M, Aosaar J, Sõber J, Lõhmus K (2014) The effects of elevated atmospheric humidity on soil respiration components in a young silver birch forest. Agric For Meteorol 194:167–174. doi:10.1016/j.agrformet.2014.04.003

    Article  Google Scholar 

  49. Kuokkanen K, Yan SC, Niemelä P (2003) Effects of elevated CO2 and temperature on the leaf chemistry of birch Betula pendula (Roth) and the feeding behaviour of the weevil Phyllobius maculicornis. Agric For Entomol 5:209–217. doi:10.1046/j.1461-9563.2003.00177.x

    Article  Google Scholar 

  50. Kupper P, Sõber J, Sellin A, Lõhmus K, Tullus A, Räim O, Lubenets K, Tulva I, Uri V, Zobel M, Kull O, Sõber A (2011) An experimental facility for free air humidity manipulation (FAHM) can alter water flux through deciduous tree canopy. Environ Exp Bot 72:432–438. doi:10.1016/j.envexpbot.2010.09.003

    Article  Google Scholar 

  51. Kuwagata T, Ishikawa-Sakurai J, Hayashi H, Nagasuga K, Fukushi K, Ahamed A, Takasugi K, Katsuhara M, Murai-Hatano M (2012) Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants. Plant Cell Physiol 53:1418–1431. doi:10.1093/pcp/pcs087

    CAS  Article  Google Scholar 

  52. La Porta N, Capretti P, Thomsen IM, Kasanen R, Hietala AM, Von Weissenberg K (2008) Forest pathogens with higher damage potential due to climate change in Europe. Can J Plant Pathol 30:177–195. doi:10.1080/07060661.2008.10540534

    Article  Google Scholar 

  53. Landsberg J, Sands P (2011) Physiological ecology of forest production. Principles, processes and models. Academic Press, London

    Google Scholar 

  54. Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876. doi:10.1093/jxb/erp096

    CAS  Article  Google Scholar 

  55. Lei H, Gartner BL, Milota MR (1997) Effect of growth rate on the anatomy, specific gravity, and bending properties of wood from 7-year-old red alder (Alnus rubra). Can J For Res 27:80–85. doi:10.1139/x96-165

    Article  Google Scholar 

  56. Lendzion J, Leuschner C (2008) Growth of European beech (Fagus sylvatica L) seedlings is limited by elevated atmospheric vapour pressure deficits. For Ecol Manage 256:648–655. doi:10.1016/j.foreco.2008.05.008

    Article  Google Scholar 

  57. Lévesque M, Rigling A, Bugmann H, Weber P, Brang P (2014) Growth response of five co-occurring conifers to drought across a wide climatic gradient in Central Europe. Agric For Meteorol 197:1–12. doi:10.1016/j.agrformet.2014.06.001

    Article  Google Scholar 

  58. Levin M, Lemcoff JH, Cohen S, Kapulnik Y (2007) Low air humidity increases leaf-specific hydraulic conductance of Arabidopsis thaliana (L.) Heynh (Brassicaceae). J Exp Bot 58:3711–3718. doi:10.1093/jxb/erm220

    CAS  Article  Google Scholar 

  59. Lihavainen J, Ahonen V, Keski-Saari S, Kontunen-Soppela S, Oksanen E, Keinänen M (2016a) Low vapour pressure deficit affects nitrogen nutrition and foliar metabolites of silver birch. J Exp Bot. doi:10.1093/jxb/erw218

    Google Scholar 

  60. Lihavainen J, Keinänen M, Keski-Saari S, Kontunen-Soppela S, Sõber A, Oksanen E (2016b) Artificially decreased vapour pressure deficit in field conditions modifies foliar metabolite profiles of birch and aspen. J Exp Bot. doi:10.1093/jxb/erw219

    Google Scholar 

  61. Lillo C, Lea US, Ruoff P (2008) Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ 31:587–601. doi:10.1111/j.1365-3040.2007.01748.x

    CAS  Article  Google Scholar 

  62. Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolström M, Lexer MJ, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manag 259:698–709. doi:10.1016/j.foreco.2009.09.023

    Article  Google Scholar 

  63. Lindner M, Fitzgerald JB, Zimmermann NE, Reyer C, Delzon S, van der Maaten E, Schelhaas M-J, Lasch P, Eggers J, van der Maaten-Theunissen M, Suckow F, Psomas A, Poulter B, Hanewinkel M (2014) Climate change and European forests: What do we know, what are the uncertainties, and what are the implications for forest management? J Environ Manag 146:69–83. doi:10.1016/j.jenvman.2014.07.030

    Article  Google Scholar 

  64. Liu B, Rennenberg H, Kreuzwieser J (2015) Hypoxia affects nitrogen uptake and distribution in young poplar (Populus × canescens) trees. PLoS ONE 10:e0136579. doi:10.1371/journal.pone.0136579

    Article  CAS  Google Scholar 

  65. Lonsdale D, Gibbs JN (1996) Effects of climate change on fungal diseases in trees. In: Frankland JC, Magan N, Gadd GM (eds) Fungi and environmental change. Cambridge University Press, Cambridge, pp 1–19

  66. Løvdal T, Olsen KM, Slimestad R, Verheul M, Lillo C (2010) Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 71:605–613. doi:10.1016/j.phytochem.2009.12.014

    Article  CAS  Google Scholar 

  67. Madden LV (1997) Effects of rain on splash dispersal of fungal pathogens. Can J Plant Pathol 19(2):225–230. doi:10.1080/07060669709500557

    Article  Google Scholar 

  68. Mäenpää M, Riikonen J, Kontunen-Soppela S, Rousi M, Oksanen E (2011) Vertical profiles reveal impact of ozone and temperature on carbon assimilation of Betula pendula and Populus tremula. Tree Physiol 31:808–818. doi:10.1093/treephys/tpr075

    Article  CAS  Google Scholar 

  69. Magnani F, Mencuccini M, Grace J (2000) Age-related decline in stand productivity: the role of structural acclimation under hydraulic constraints. Plant Cell Environ 23:251–263. doi:10.1046/j.1365-3040.2000.00537.x

    Article  Google Scholar 

  70. Maier CA, Zarnoch SJ, Dougherty PM (1998) Effects of temperature and tissue nitrogen on dormant season stem and branch maintenance respiration in a young loblolly pine (Pinus taeda) plantation. Tree Physiol 18:11–20. doi:10.1093/treephys/18.1.11

    Article  Google Scholar 

  71. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London

    Google Scholar 

  72. McDowell N, Barnard H, Bond BJ, Hinckley T, Hubbard RM, Ishii H, Köstner B, Magnani F, Marshall JD, Meinzer FC, Phillips N, Ryan MG, Whitehead D (2002) The relationship between tree height and leaf area: sapwood area ratio. Oecologia 132:12–20. doi:10.1007/s00442-002-0904-x

    CAS  Article  Google Scholar 

  73. Meinzer FC (2003) Functional convergence in plant responses to the environment. Oecologia 134:1–11. doi:10.1007/s00442-002-1088-0

    Article  Google Scholar 

  74. Melcher PJ, Holbrook NM, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L (2012) Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods Ecol Evol 3:685–694. doi:10.1111/j.2041-210X.2012.00204.x

    Article  Google Scholar 

  75. Mielke MS, de Almeida AAF, Gomes FP, Aguilar MAG, Mangabeira PO (2003) Leaf gas exchange, chlorophyll fluorescence and growth responses of Genipa americana seedlings to soil flooding. Environ Exp Bot 50:221–231. doi:10.1016/S0098-8472(03)00036-4

    CAS  Article  Google Scholar 

  76. Neuman DS, Rood SB, Smit BA (1990) Does cytokinin transport from root-to-shoot in the xylem sap regulate leaf responses to root hypoxia? J Exp Bot 41:1325–1333. doi:10.1093/jxb/41.10.1325

    CAS  Article  Google Scholar 

  77. Niglas A, Kupper P, Tullus A, Sellin A (2014) Responses of sap flow, leaf gas exchange and growth of hybrid aspen to elevated atmospheric humidity under field conditions. AoB Plants 6:plu021. doi:10.1093/aobpla/plu021

  78. Niglas A, Alber M, Suur K, Jasińska AK, Kupper P, Sellin A (2015) Does increased air humidity affect stomatal morphology and functioning in hybrid aspen? Botany 93:243–250. doi:10.1139/cjb-2015-0004

    Article  Google Scholar 

  79. Niu S, Luo Y, Li D, Gao S, Xia J, Li J, Smith MD (2014) Plant growth and mortality under climatic extremes: an overview. Environ Exp Bot 98:13–19. doi:10.1016/j.envexpbot.2013.10.004

    Article  Google Scholar 

  80. Olano JM, Arzac A, Garcia-Cervigon AI, Arx G, Rozas V (2013) New star on the stage: amount of ray parenchyma in tree rings shows a link to climate. New Phytol 198:486–495. doi:10.1111/nph.12113

    Article  Google Scholar 

  81. Oliva J, Stenlid J, Martínez-Vilalta J (2014) The effect of fungal pathogens on the water and carbon economy of trees: implications for drought-induced mortality. New Phytol 203:1028–1035. doi:10.1111/nph.12857

    CAS  Article  Google Scholar 

  82. Pallardy SG (2008) Physiology of woody plants. Academic Press, Burlington

    Google Scholar 

  83. Parts K, Tedersoo L, Lõhmus K, Kupper P, Rosenvald K, Sõber A, Ostonen I (2013) Increased air humidity and understory composition shape short root traits and the colonizing ectomycorrhizal fungal community in silver birch stands. For Ecol Manage 310:720–728. doi:10.1016/j.foreco.2013.09.017

    Article  Google Scholar 

  84. Pasho E, Camarero JJ, de Luis M, Vicente-Serrano SM (2012) Factors driving growth responses to drought in Mediterranean forests. Eur J For Res 131:1797–1807. doi:10.1007/s10342-012-0633-6

    Article  Google Scholar 

  85. Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400. doi:10.1093/jexbot/52.360.1383

    CAS  Article  Google Scholar 

  86. Pautasso M, Döring TF, Garbelotto M, Pellis L, Jeger MJ (2012) Impacts of climate change on plant diseases—opinions and trends. Eur J Plant Pathol 133:295–313. doi:10.1007/s10658-012-9936-1

    Article  Google Scholar 

  87. Plassard C, Dell B (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiol 30:1129–1139. doi:10.1093/treephys/tpq063

    CAS  Article  Google Scholar 

  88. Poorter L, McDonald I, Alarcón A, Fichtler E, Licona J-C, Peña-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492. doi:10.1111/j.1469-8137.2009.03092.x

    Article  Google Scholar 

  89. Possen BJHM, Oksanen E, Rousi M, Ruhanen H, Ahonen V, Tervahauta A, Heinonen J, Heiskanen J, Kärenlampi S, Vapaavuori E (2011) Adaptability of birch (Betula pendula Roth) and aspen (Populus tremula L.) genotypes to different soil moisture conditions. For Ecol Manage 262:1387–1399. doi:10.1016/j.foreco.2011.06.035

    Article  Google Scholar 

  90. Räisänen J, Hansson U, Ullerstig A, Döscher R, Graham LP, Jones C, Meier HEM, Samuelsson P, Willén U (2004) European climate in the late twenty-first century: regional simulations with two driving global models and two forcing scenarios. Clim Dyn 22:13–31. doi:10.1007/s00382-003-0365-x

    Article  Google Scholar 

  91. Riikonen J, Holopainen T, Oksanen E, Vapaavuori E (2005) Leaf photosynthetic characteristics of silver birch during three years of exposure to elevated concentrations of CO2 and O3 in the field. Tree Physiol 25:621–632. doi:10.1093/treephys/25.5.621

    CAS  Article  Google Scholar 

  92. Rodríguez-Calcerrada J, López R, Salomón R, Gordaliza GG, Valbuena-Carabaña M, Oleksyn J, Gil L (2015) Stem CO2 efflux in six co-occurring tree species: underlying factors and ecological implications. Plant Cell Environ 38:1104–1115. doi:10.1111/pce.12463

    Article  CAS  Google Scholar 

  93. Rosenvald K, Tullus A, Ostonen I, Uri V, Kupper P, Aosaar J, Varik M, Sõber J, Niglas A, Hansen R, Rohula G, Kukk M, Sõber A, Lõhmus K (2014) The effect of elevated air humidity on young silver birch and hybrid aspen biomass allocation and accumulation—acclimation mechanisms and capacity. For Ecol Manage 330:252–260. doi:10.1016/j.foreco.2014.07.016

    Article  Google Scholar 

  94. Ryan MG (1990) Growth and maintenance respiration in stems of Pinus contorta and Picea engelmannii. Can J For Res 20:48–57. doi:10.1139/x90-008

    Article  Google Scholar 

  95. Ryan MG (1991) The effect of climate change on plant respiration. Ecol Appl 1:157–167. doi:10.2307/1941808

    Article  Google Scholar 

  96. Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381. doi:10.1111/j.1365-3040.2005.01478.x

    Article  Google Scholar 

  97. Saxe H, Ellsworth DS, Health J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139:395–436. doi:10.1046/j.1469-8137.1998.00221.x

    Article  Google Scholar 

  98. Saxe H, Cannell MGR, Johnsen Ø, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–400. doi:10.1046/j.1469-8137.2001.00057.x

    CAS  Article  Google Scholar 

  99. Sellin A, Alber M (2013) Impact of increasing atmospheric humidity on leaf vascular system and hydraulic conductance. In: Programme and abstracts of the III International Conference on plant vascular biology. Helsinki: University of Helsinki, p 62

  100. Sellin A, Kupper P (2013) Responses of gas exchange and plant hydraulic conductance to water deficit in silver birch trees growing under increasing atmospheric humidity. Geophys Res Abstr 15:EGU2013-3007-2

  101. Sellin A, Õunapuu E, Kaurilind E, Alber M (2012) Size-dependent variability of leaf and shoot hydraulic conductance in silver birch. Trees 26:821–831. doi:10.1007/s00468-011-0656-5

    Article  Google Scholar 

  102. Sellin A, Tullus A, Niglas A, Õunapuu E, Karusion A, Lõhmus K (2013) Humidity-driven changes in growth rate, photosynthetic capacity, hydraulic properties and other functional traits in silver birch (Betula pendula). Ecol Res 28:523–535. doi:10.1007/s11284-013-1041-1

    CAS  Article  Google Scholar 

  103. Sellin A, Niglas A, Õunapuu-Pikas E, Kupper P (2014) Rapid and long-term effects of water deficit on gas exchange and hydraulic conductance of silver birch trees grown under varying atmospheric humidity. BMC Plant Biol 14:72. doi:10.1186/1471-2229-14-72

    Article  Google Scholar 

  104. Sellin A, Rosenvald K, Õunapuu-Pikas E, Tullus A, Ostonen I, Lõhmus K (2015) Elevated air humidity affects hydraulic traits and tree size but not biomass allocation in young silver birches (Betula pendula). Front Plant Sci 6:860. doi:10.3389/fpls.2015.00860

    Article  Google Scholar 

  105. Smit B, Stachowiak M, Van Volkenburgh E (1989) Cellular processes limiting leaf growth in plants under hypoxic root stress. J Exp Bot 40:89–94. doi:10.1093/jxb/40.1.89

    Article  Google Scholar 

  106. Smit BA, Neuman DS, Stachowiak ML (1990) Root hypoxia reduces leaf growth. Role of factors in the transpiration stream. Plant Physiol 92:1021–1028. doi:10.1104/pp.92.4.1021

    CAS  Article  Google Scholar 

  107. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20. doi:10.1104/pp.103.024380

    CAS  Article  Google Scholar 

  108. Sonnewald U, Willmitzer L (1992) Molecular approaches to sink-source interactions. Plant Physiol 99:1267–1270. doi:10.1104/pp.99.4.1267

    CAS  Article  Google Scholar 

  109. Spicer R, Holbrook NM (2007) Parenchyma cell respiration and survival in secondary xylem: does metabolic activity decline with cell age? Plant Cell Environ 30:934–943. doi:10.1111/j.1365-3040.2007.01677.x

    CAS  Article  Google Scholar 

  110. Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14:741–762. doi:10.1111/j.1365-3040.1991.tb01440.x

    CAS  Article  Google Scholar 

  111. Sturrock RN, Frankel SJ, Brown AV, Hennon PE, Kliejunas JT, Lewis KJ, Worrall JJ, Woods AJ (2011) Climate change and forest diseases. Plant Pathol 60:133–149. doi:10.1111/j.1365-3059.2010.02406.x

    Article  Google Scholar 

  112. Thornton PK, Ericksen PJ, Herrero M, Challinor AJ (2014) Climate variability and vulnerability to climate change: a review. Glob Change Biol 20:3313–3328. doi:10.1111/gcb.12581

    Article  Google Scholar 

  113. Tullus A, Kupper P, Sellin A, Parts L, Sõber J, Tullus T, Lõhmus K, Sõber A, Tullus H (2012a) Climate change at northern latitudes: rising atmospheric humidity decreases transpiration, N-uptake and growth rate of hybrid aspen. PLoS ONE 7:e42648. doi:10.1371/journal.pone.0042648

    CAS  Article  Google Scholar 

  114. Tullus A, Rytter L, Tullus T, Weih M, Tullus H (2012b) Short-rotation forestry with hybrid aspen (Populus tremula L. & #x00D7; P. tremuloides Michx.) in Northern Europe. Scand J For Res 27:10–29. doi:10.1080/02827581.2011.628949

    Article  Google Scholar 

  115. Tullus, A, Sellin A, Kupper P, Lutter R, Pärn L, Jasińska AK, Alber M, Kukk M, Tullus T, Tullus H, Lõhmus K, Sõber A (2014) Increasing air humidity—a climate trend predicted for northern latitudes—alters the chemical composition of stemwood in silver birch and hybrid aspen. Silva Fenn 48:article id 1107. doi:10.14214/sf.1107

  116. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Berlin

    Book  Google Scholar 

  117. Vasaitis R (2013) Heart rots, sap rots and canker rots. In: Gonthier P, Nicolotti G (eds) Infectious forest diseases. CABI Publishing, wallingford, pp 197–229. doi:10.1079/9781780640402.0197

  118. Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688. doi:10.1093/treephys/tpq015

    Article  Google Scholar 

  119. Weemstra M, Eilmann B, Sass-Klaassen UGW, Sterck FJ (2013) Summer droughts limit tree growth across 10 temperate species on a productive forest site. For Ecol Manage 306:142–149. doi:10.1016/j.foreco.2013.06.007

    Article  Google Scholar 

  120. Whiting EC, Rizzo DM (1999) Effect of water potential on radial colony growth of Armillaria mellea and A. gallica isolates in culture. Mycologia 91:627–635. doi:10.2307/3761248

    Article  Google Scholar 

  121. Yamamoto F, Kozlowski TT, Wolter KE (1987) Effect of flooding on growth, stem anatomy, and ethylene production of Pinus halepensis seedlings. Can J For Res 17:69–79. doi:10.1139/x87-013

    CAS  Article  Google Scholar 

  122. Zang C, Hartl-Meier C, Dittmar C, Rothe A, Menzel A (2014) Patterns of drought tolerance in major European temperate forest trees: climatic drivers and levels of variability. Glob Change Biol 20:3767–3779. doi:10.1111/gcb.12637

    Article  Google Scholar 

  123. Zhang Y-J, Meinzer FC, Hao G-Y, Scholz FG, Bucci SJ, Takahashi FSC, Villalobos-Vega R, Giraldo JP, Cao KF, Hoffmann WA, Goldstein G (2009) Size-dependent mortality in a Neotropical savanna tree: the role of height-related adjustments in hydraulic architecture and carbon allocation. Plant Cell Environ 32:1456–1466. doi:10.1111/j.1365-3040.2009.02012.x

    CAS  Article  Google Scholar 

  124. Zwieniecki MA, Secchi F (2015) Threats to xylem hydraulic function of trees under ‘new climate normal’ conditions. Plant Cell Environ 38:1713–1724. doi:10.1111/pce.12412

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the Estonian Ministry of Education and Research (Target Financing Project SF0180025s12 and Institutional Research Funding IUT34-9), by the Academy of Finland (Project No. 250636) and by the European Union through the European Regional Development Fund (Project No. 3.2.0802.11-0043 ‘BioAtmos’ and Centre of Excellence in Environmental Adaptation). We are grateful to Sarita Keski-Saari and Sari Kontunen-Soppela for their contributions to the metabolite research and for comments that helped improve the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Arne Sellin.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sellin, A., Alber, M., Keinänen, M. et al. Growth of northern deciduous trees under increasing atmospheric humidity: possible mechanisms behind the growth retardation. Reg Environ Change 17, 2135–2148 (2017). https://doi.org/10.1007/s10113-016-1042-z

Download citation

Keywords

  • Atmospheric humidity
  • Climate change
  • Deciduous trees
  • Growth decline
  • Metabolic stress
  • Nutrient uptake